Evidence that Inositol Polyphosphate 4-Phosphatase Type II Is a Tumor Suppressor that Inhibits PI3K Signaling

Cancer Cell

Volumn 16, Issue 2, 2009, Pages 115-125

  Gewinner, Christina ^a   Wang, Zhigang C ^b   Richardson, Andrea ^b   Teruya Feldstein, Julie ^c   Etemadmoghadam, Dariush ^d   Bowtell, David ^d   Barretina, Jordi ^e   Lin, William M ^e   Rameh, Lucia ^f   Salmena, Leonardo ^b   Pandolfi, Pier Paolo ^b   Cantley, Lewis C ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

CELLCYCLE

Indexed keywords

INOSITOL POLYPHOSPHATE 4 PHOSPHATASE TYPE II; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER INHIBITION; CANCER SURVIVAL; CELL AGING; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; GENE OVEREXPRESSION; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; INTRADUCTAL CARCINOMA; MOUSE; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT;

EID: 67651148274     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.06.006     Document Type: Article

References (49)

1. Auger K.R., Serunian L.A., Soltoff S.P., Libby P., and Cantley L.C. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 57 (1989) 167-175
2. Barnache S., Le Scolan E., Kosmider O., Denis N., and Moreau-Gachelin F. Phosphatidylinositol 4-phosphatase type II is an erythropoietin-responsive gene. Oncogene 25 (2006) 1420-1423
3. Bergamaschi A., Kim Y.H., Wang P., Sorlie T., Hernandez-Boussard T., Lonning P.E., Tibshirani R., Borresen-Dale A.L., and Pollack J.R. Distinct patterns of DNA copy number alteration are associated with different clinicopathological features and gene-expression subtypes of breast cancer. Genes Chromosomes Cancer 45 (2006) 1033-1040
4. Braig M., Lee S., Loddenkemper C., Rudolph C., Peters A.H., Schlegelberger B., Stein H., Dorken B., Jenuwein T., and Schmitt C.A. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436 (2005) 660-665
5. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 296 (2002) 1655-1657
6. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., Koutcher J.A., Scher H.I., Ludwig T., Gerald W., et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436 (2005) 725-730
7. Chin S.F., Wang Y., Thorne N.P., Teschendorff A.E., Pinder S.E., Vias M., Naderi A., Roberts I., Barbosa-Morais N.L., Garcia M.J., et al. Using array-comparative genomic hybridization to define molecular portraits of primary breast cancers. Oncogene 26 (2007) 1959-1970
8. Collado M., Gil J., Efeyan A., Guerra C., Schuhmacher A.J., Barradas M., Benguria A., Zaballos A., Flores J.M., Barbacid M., et al. Tumour biology: senescence in premalignant tumours. Nature 436 (2005) 642
9. Courtois-Cox S., Genther Williams S.M., Reczek E.E., Johnson B.W., McGillicuddy L.T., Johannessen C.M., Hollstein P.E., MacCollin M., and Cichowski K. A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 10 (2006) 459-472
10. Dankort D., Filenova E., Collado M., Serrano M., Jones K., and McMahon M. A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors. Genes Dev. 21 (2007) 379-384
11. Debnath J., Muthuswamy S.K., and Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30 (2003) 256-268
12. Di Cristofano A., Pesce B., Cordon-Cardo C., and Pandolfi P.P. PTEN is essential for embryonic development and tumour suppression. Nat. Genet. 19 (1998) 348-355
13. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92 (1995) 9363-9367
14. Engelman J.A., Luo J., and Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7 (2006) 606-619
15. Franke T.F., Kaplan D.R., Cantley L.C., and Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275 (1997) 665-668
16. Etemadmoghadam D., deFazio A., Beroukhim R., Mermel C., George G., Getz G., Tothill R., Okamoto A., Raeder M.B., Harnett P., et al. Integrated genome-wide DNA copy number and expression analysis identifies distinct mechanisms of primary chemoresistance in ovarian carcinomas. Clin. Cancer Res. 15 (2009) 1417-1427
17. Frech M., Andjelkovic M., Ingley E., Reddy K.K., Falck J.R., and Hemmings B.A. High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/protein kinase B and their influence on kinase activity. J. Biol. Chem. 272 (1997) 8474-8481
18. Gilby D.C., Goodeve A.C., Winship P.R., Valk P.J., Delwel R., and Reilly J.T. Gene structure, expression profiling and mutation analysis of the tumour suppressor SHIP1 in Caucasian acute myeloid leukaemia. Leukemia 21 (2007) 2390-2393
19. Hahn W.C., and Weinberg R.A. Modelling the molecular circuitry of cancer. Nat. Rev. Cancer 2 (2002) 331-341
20. Johannsdottir H.K., Johannesdottir G., Agnarsson B.A., Eerola H., Arason A., Johannsson O.T., Heikkila P., Egilsson V., Olsson H., Borg A., et al. Deletions on chromosome 4 in sporadic and BRCA mutated tumors and association with pathological variables. Anticancer Res. 24 (2004) 2681-2687
21. Kapp A.V., Jeffrey S.S., Langerod A., Borresen-Dale A.L., Han W., Noh D.Y., Bukholm I.R., Nicolau M., Brown P.O., and Tibishirani R. Discovery and validation of breast cancer subtypes. BMC Genomics 7 (2006) 231
22. Kishimoto H., Hamada K., Saunders M., Backman S., Sasaki T., Nakano T., Mak T.W., and Suzuki A. Physiological functions of Pten in mouse tissues. Cell Struct. Funct. 28 (2003) 11-21
23. Klippel A., Kavanaugh W.M., Pot D., and Williams L.T. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17 (1997) 338-344
24. Krypuy M., Ahmed A.A., Etemadmoghadam D., Hyland S.J., Australian Ovarian Cancer Study Group, deFazio A., Fox S.B., Brenton J.D., Bowtell D.D., and Dobrovic A. High resolution melting for mutation scanning of TP53 exons 5-8. BMC Cancer 7 (2007) 168
25. Lee J.M., Dedhar S., Kalluri R., and Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172 (2006) 973-981
26. Lin W.M., Baker A.C., Beroukhim R., Winckler W., Feng W., Marmion J.M., Laine E., Greulich H., Tseng H., Gates C., et al. Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res. 68 (2008) 664-673
27. Mandl A., Sarkes D., Carricaburu V., Jung V., and Rameh L. Serum withdrawal-induced accumulation of phosphoinositide 3-kinase lipids in differentiating 3T3-L6 myoblasts: distinct roles for Ship2 and PTEN. Mol. Cell. Biol. 27 (2007) 8098-8112
28. Manning B.D., and Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 129 (2007) 1261-1274
29. Naylor T.L., Greshock J., Wang Y., Colligon T., Yu Q.C., Clemmer V., Zaks T.Z., and Weber B.L. High resolution genomic analysis of sporadic breast cancer using array-based comparative genomic hybridization. Breast Cancer Res. 7 (2005) R1186-R1198
30. Nogueira V., Park Y., Chen C., Xu P., Chen M., Tonic I., Unterman T., and Hay N. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 14 (2008) 458-470
31. Norris F.A., Atkins R.C., and Majerus P.W. The cDNA cloning and characterization of inositol polyphosphate 4-phosphatase type II. Evidence for conserved alternative splicing in the 4-phosphatase family. J. Biol. Chem. 272 (1997) 23859-23864
32. Norris F.A., Auethavekiat V., and Majerus P.W. The isolation and characterization of cDNA encoding human and rat brain inositol polyphosphate 4-phosphatase. J. Biol. Chem. 270 (1995) 16128-16133
33. Ong C.J., Ming-Lum A., Nodwell M., Ghanipour A., Yang L., Williams D.E., Kim J., Demirjian L., Qasimi P., Ruschmann J., et al. Small-molecule agonists of SHIP1 inhibit the phosphoinositide 3-kinase pathway in hematopoietic cells. Blood 110 (2007) 1942-1949
34. Ory D.S., Neugeboren B.A., and Mulligan R.C. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc. Natl. Acad. Sci. USA 93 (1996) 11400-11406
35. Plas D.R., and Thompson C.B. Akt-dependent transformation: there is more to growth than just surviving. Oncogene 24 (2005) 7435-7442
36. Richardson A.L., Wang Z.C., De Nicolo A., Lu X., Brown M., Miron A., Liao X., Iglehart J.D., Livingston D.M., and Ganesan S. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9 (2006) 121-132
37. Saal L.H., Gruvberger-Saal S.K., Persson C., Lovgren K., Jumppanen M., Staaf J., Jonsson G., Pires M.M., Maurer M., Holm K., et al. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat. Genet. 40 (2008) 102-107
38. Scheid M.P., Huber M., Damen J.E., Hughes M., Kang V., Neilsen P., Prestwich G.D., Krystal G., and Duronio V. Phosphatidylinositol (3,4,5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3,4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J. Biol. Chem. 277 (2002) 9027-9035
39. Scheid M.P., and Woodgett J.R. Phosphatidylinositol 3′ kinase signaling in mammary tumorigenesis. J. Mammary Gland Biol. Neoplasia 6 (2001) 83-99
40. Sharrard R.M., and Maitland N.J. Regulation of protein kinase B activity by PTEN and SHIP2 in human prostate-derived cell lines. Cell. Signal. 19 (2007) 129-138
41. Sleeman M.W., Wortley K.E., Lai K.M., Gowen L.C., Kintner J., Kline W.O., Garcia K., Stitt T.N., Yancopoulos G.D., Wiegand S.J., and Glass D.J. Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11 (2005) 199-205
42. Song M.S., Salmena L., Carracedo A., Egia A., Lo-Coco F., Teruya-Feldstein J., and Pandolfi P.P. The deubiquitinylation and localization of PTEN are regulated by a HAUSPA-PML network. Nature 455 (2008) 813-817
43. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 98 (2001) 10869-10874
44. Sterian A., Kan T., Berki A.T., Mori Y., Olaru A., Schulmann K., Sato F., Wang S., Paun B., Cai K., et al. Mutational and LOH analyses of the chromosome 4q region in esophageal adenocarcinoma. Oncology 70 (2006) 168-172
45. Vazquez F., and Sellers W.R. The PTEN tumor suppressor protein: an antagonist of phosphoinositide 3-kinase signaling. Biochim. Biophys. Acta 1470 (2000) M21-M35
46. Vivanco I., and Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2 (2002) 489-501
47. Westbrook T.F., Martin E.S., Schlabach M.R., Leng Y., Liang A.C., Feng B., Zhao J.J., Roberts T.M., Mandel G., Hannon G.J., et al. A genetic screen for candidate tumor suppressors identifies REST. Cell 121 (2005) 837-848
48. Whitman M., Kaplan D., Roberts T., and Cantley L. Evidence for two distinct phosphatidylinositol kinases in fibroblasts. Implications for cellular regulation. Biochem. J. 247 (1987) 165-174
49. Zhao J.J., Gjoerup O.V., Subramanian R.R., Cheng Y., Chen W., Roberts T.M., and Hahn W.C. Human mammary epithelial cell transformation through the activation of phosphatidylinositol 3-kinase. Cancer Cell 3 (2003) 483-495